One of the most distinctive features of ceratopsian dinosaurs is the conspicuous bony frill, formed from the parietal and squamosal bones, that projected backwards (and sometimes upwards too) from the rear margin of the skull.

Typically decorated around their edges by semi-circular bones called epoccipitals, and sometimes sporting horns, spikes or mid-line keels, frills were a fundamental part of the skull: this means that, whenever the animal moved its head up, or down, or to the side, the whole frill moved too. The fact that the ceratopsian occipital condyle is damn-near spherical shows that the head-neck joint was particularly mobile, and that these dinosaurs were well able to dip the snout right down to the ground, to throw the head from side to side, and to point the snout upwards until the frill rested on the shoulders.

Because the supratemporal fenestrae (the openings at the back of the skull that, at their edges, anchor various jaw muscles*) open on the surface of the frill, at least some of the jaw musculature must have extended on to the frill. In normal tetrapods, these muscles are restricted to the areas just around the fenestrae… but ceratopsians aren’t normal tetrapods: the bones at the rear of the skull are horrendously modified. Could, therefore, the massive frill be a specialisation allowing hypertrophied jaw musculature? A number of authors have proposed exactly this, and have imagined ceratopsian jaw musculature extending right across the frill, all the way to the rear margin. As Dodson (1996) explained, the logic behind this super-muscled frill was flawed: animals do not need gigantic, super-long jaw-closing muscles to have a powerful bite, and the surface texture of the frill is not consistent with a covering of musculature. It seems that the musculature was, most likely, restricted to the areas just around the supratemporal fenestrae [adjacent reconstructions of jaw musculature in Chasmosaurus and Styracosaurus from Dodson (1996). Note that Styracosaurus is now known to have a shorter nasal horn than the one shown here].

* Note that the ‘windows’ on the frills of most ceratopsians are not the same thing as the supratemporal fenestrae.

However, back when the hypothesis of extensive frill musculature was considered reasonable, a truly extreme version was proposed by John McLoughlin in his book Archosauria: : A New Look at the Old Dinosaur. McLoughlin (1979) proposed that the frill did not just anchor musculature: it was essentially buried by a massive amount of muscle that extended around the back of the skull, and across the shoulders too. I never saw John’s book until I was in my 20s, and only knew of his ‘alternative’ look for ceratopsians thanks to a picture [shown here] in David Lambert’s Collins Guide to Dinosaurs (one of my favourite childhood books). Some of his reconstructions, which look very strange today, are shown here: his Triceratops is shown above, and his Chasmosaurus is below.

While these reconstructions are improbable for the reasons mentioned above, they can also be considered illogical because they would mean that the frill – and hence the entire head – was virtually immobile, and held firmly in place against the shoulders. The projecting epoccipitals, knobs and other structures on the frill surfaces and edges also show that the frill cannot have been submerged in soft tissue. Furthermore, the frills of some ceratopsid ceratopsians – notable examples include Pentaceratops and Agujaceratops – are so long, and so strongly inclined upwards relative to the long axis of the skull, that there can be no doubt that they stood well up above the shoulders in life, and cannot have been ‘tied’ to the thorax by soft tissues. While some modern lizards sport bony frills that are connected to the thorax by skin webs (the iguanian Corytophanes is perhaps the best example: see the photo I used here), the frills in these animals are narrow, sheet like structures. Certain chameleons do have wider, more ceratopsian-like frills, and these are not connected by soft tissue to the animal’s back.

Well, this post started as an excuse to show some of John McLoughlin’s interesting pictures, but (like so many others) it quickly got out of hand. For previous ceratopsian posts see…

Comments

Who changed the layout so that the blockquotes now project outwards instead of inwards and cover the numbers, now on the left? I thought it was just what two or three newer ScienceBlogs had chosen, but now it’s everywhere… ~:-|

Good that there are numbers, though. Some threads were getting quite long here. 🙂

W00t! Looks like this has inadvertently turned into Neoceratopsian Week.

I’ve always found the idea of the frills being submerged in soft tissue as quite ridiculous.

Speaking of which, has the idea of Triceratops‘ frill being a protective shield been debunked in the scientific literature yet? I know it’s very unlikely that ceratopsian frills offered any effective resistance against tyrannosaur jaws, but I’m wondering if the evolution of epoccipitals and spikes was in part driven by predation from tyrannosaurs; a hungry tyrannosaur aiming for the nape would have encountered a rather prickly obstacle.

I guess a tyrannosaur would think twice before attacking that general area around the frill, especially in the case of Styracosaurus. I can envision a threatened ceratopsian bobbing and waving its head about, fending off lunges from a tyrannosaur by aiming the spikes on the frill towards its attacker’s face. This meant that a wider perimeter around the ceratopsian’s body was protected in some way; no way is the tyrannosaur going to risk a frontal attack because of the horns, and if it tries to attack from the side out of range of the horns, the epoccipitals and frills could provide some degree of protection. And for those with long spikes on the frill (e.g. Styracosaurus) or just very long frills (Pentaceratops), it might be possible to stave off the first attack from the rear, simply by having the ceratopsian raise its head all the way up, so that the frill rested firmly on the shoulders, with the spikes or the long frill itself protecting the nape (while at the same time leaving the throat exposed though).

But then of course, what about those species that did not evolve long spikes on the frills (especially many of the chasmosaurines) … I guess intraspecific display and interspecies recognition were ultimately the primary functions of the frill.

As an aside, long before the discovery of Zuniceratops and Albertaceratops, sometime in the mid-90s, I used to think that having long nasal horns was the basal condition (recall the reconstructions of Montanoceratops and Bagaceratops with a stubby little horn on the nose?), and that the chasmosaurines with their brow horns outlasted the centrosaurines because nasal horns proved ineffective against tyrannosaurs; according to my little hypothesis, as the tyrannosaurs evolved a greater degree of stereoscopic vision (compare the narrower skull of Gorgosaurus with the much wider one of Tyrannosaurus), they were finding it easier to dodge the nasal horns of centrosaurines, which provided only a single pointy end to avoid. Pachyrhinosaurus turned the sharp nasal horn into a battering ram, but it was not effective enough as a form of defense. Chasmosaurines though, with 2 pointy ends (the brow horns), were better able to repel tyrannosaur attacks. I think I was only 13 or 14 then. =)

I’ve always been intrigued by the fact that the centrosaurines seem to have been much more common than centrosaurines within the Campanian, only to show signs of decline in the Early Maastrichtian (only Pachyrhinosaurus left), while the chasmosaurines had always been around, but truly rose to dominance after the centrosaurines snuffed it. There’s also the fact that the chasmosaurines seem to have representatives further to the south (e.g. Pentaceratops in New Mexico, Agujaceratops in Texas), while the centrosaurines ranged further to the north (Pachyrhinosaurus), although I’m not sure if that’s still the case now. If the chasmosaurines were a more southerly group and the centrosaurines were more northerly, I wonder if it could have been due to differences in ecological preferences. I’ve read somewhere that centrosaurines may have been more gregarious and preferred drier uplands, while chasmosaurines lived in smaller herds in the moister lowlands (hmm… or was it the other way around).

Although he was drawing rather ridiculous ceratopsids, I would like to mention that he was one of the first (maybe THE first) drawing feathered theropods. Unfortunately, it appears that none of these drawings is easily found on the internet…

Darren, I agree with your conclusions (the ‘ball-and-socket’ articulation of the head/neck joint clinches it for me – and for feeding, display and defence, such a highly-manoeuvrable ceratopsian head makes perfect sense: to be able to raise the frill for maximum visibility; to angle the shearing beak so as to grip and snip off variously-angled stems of vegetation; to direct spikes at an aggressor, etc.
The ‘stiff-neck’ idea seems clearly an implausible impediment in all these areas.
Still, those are neat drawings. Sometimes an idea is worth raising (and illustrating) simply for its clear refutation.

The drawings raise another point – or rather two points – eyes! Two of these ceratopsian illustrations have a horizontal oval pupil (goat-like), another has the non-committal ‘dark orb with highlight’.
(I opted for the former in my illustration here.)

I wonder if there has been any systematic analysis of pupil type, among various kinds of animal / kinds of habitat (eg plains/forest, terrestrial/aquatic/amphibious) / kinds of lifestyle (diurnal/nocturnal), and so any conclusions reachable about likely pupil-type in extinct forms?
Existing fauna are very varied (and some downright weird) in pupil/iris form. I guess extinct forms could be similarly varied. For some fossil forms, the presence and preservation of sclerotic rings (eye-bones!) may throw light..

The error in the 100% muscled frill is obvious simply based on muscle physiology – muscle force is dependent upon cross-sectional area, not length. A long muscle generates the same force, but costs more energy, because the *whole* length must be activated. Long muscles can do more work and generate more power, but power isn’t a big deal for herbivores and work is constrained by the displacement of the ceratopsian jaw. Muscle pennation may have been involved (as seen in the more reduced-muscle illustration), but at such a great extreme, especially for monsters like Torosaurus, it would have exceeded any required bite force by orders of magnitude.

The horizontal pupil looks cool and apparently would make sense for a herbivore feeding in open areas and would afford an almost 360 view…but wouldn’t the large heads and frills of most ceratopsians block that view anyway? So…if an basal ceratopsian had that eye structure, would it have changed once the ornamentation became so elaborate or would it be retained?

I wonder if there has been any systematic analysis of pupil type, among various kinds of animal / kinds of habitat (eg plains/forest, terrestrial/aquatic/amphibious) / kinds of lifestyle (diurnal/nocturnal), and so any conclusions reachable about likely pupil-type in extinct forms?

You want publications on vertebrate pupil shapes and how they differ in different habitats? See Malmström & Kröger (2006) and Mass & Supin (2007), for starters (these references just off the top of my head). And there is also, of course, the classic and still useful treatise by Walls (1942). I’m not aware of any study specifically dealing with the reconstruction of pupil shape in wholly extinct taxa, though.

“The Sb platform underwent some style changes yesterday: they were not implemented by individual bloggers. I suppose it’s useful to number the comments, but I’m not (yet) too keen on the way it looks.”

I agree, not only does the new style look rather ugly, especially the new font style, but it reminds me too much of Pharyngula, and its swampload of weird comments, especially about bacon. Next I suppose they’re going to make it mandatory to register to comment on ScienceBlogs.

“but ceratopsians aren’t normal tetrapods”

Are there really any normal tetrapods? Turtles are animals that have been pulled inside out and some breathe through their butt, snakes have been rolled into a tube and lost one of their lungs, salamanders only have one neck vertebrae (or so I’ve read) and some have actually lost their lungs entirely, and there is one particularly ugly mammal which uses massive buttocks to make up for a lack of a tail, has a huge brain to the point where it cannot strengthen its jaws without affecting the brain size, and it walks upright, with basal five fingered hands. Oh, did I mention its naked?

“Speaking of which, has the idea of Triceratops’ frill being a protective shield been debunked in the scientific literature yet?”

Ironically, if there was any ceratopsian who could have used their frill for protection, it was Triceratops. Unlike other neoceratopsians, it had a solid frill. But I do agree that spines on the frill seem a much better tyrannosaur deterrent than a bony “shield”. It still seems like the frills were display or identification structures.

“while the centrosaurines ranged further to the north (Pachyrhinosaurus), although I’m not sure if that’s still the case now.”

Pachyrhinosaurus may have survived so long because it was essentially a dinosaurian “musk ox”, thriving more in the cooler climates of the far north than its kin. Surprisingly, I saw a cladogram by Dr. Michael Ryan showing Pachies and their allies (maybe we need a Pachyrhinosaurinii or something, or does it already exist?) claiming they were some of the most basal centrosaurines, more derived than Albertaceratops but less derived than Centrosaurus and its kin.

“Sometimes an idea is worth raising (and illustrating) simply for its clear refutation.”

I agree with Graham. I’ve always thought that ceratopsians had the “normal” frill that has been portrayed in popular media, but I was just wondering seeing as we really don’t have any modern animals today that have such frills. Thanks for answering my question Darren. Though what is stopping a big chunk of muscle being down there, not as massive as the ones presented above, and not sinking the frill into the flesh, but still smoothing the frill into the body. (Just wondering why it cannot be, not suggesting it is).

One other piece of evidence against the frill being completely buried in muscle is the distribution of the neurovascular impressions (which indicate a tight-fitting covering of skin, most likely). They completely cover the front of the frill in Triceratops (except for the area of insertion for the adductor muscles, of course), and also go part of the way down the back side.

The claim that the Pachyrhinosaurinii (yes, it’s a real group already) is a basal group within the centrosaurinae is news to me. I’ve always read that they’re the most derived centrosaurs. I imagine this idea comes from the fact that Albertaceratops has a bannana-shaped boss along its nasals? However, it’s really nothing like the wide, rugose bosses of Achelousaurus and Pachyrhinosaurus, which are laterally-expanded nasal horns (ontogenetically). I believe the Styracosaurus-Einiosaurus-Pachyrhinosaurinii is still well-supported phylogenetically. Could be wrong, of course.

Pachyrhinosaurus as musk ox? I like it, especially with the idea that the nasal boss was covered with a rugose musk ox-like horny sheath!

The minute I saw the headline, I knew this was going to mention McLoughlin’s stiff-necked pointillism Triceratops. Chalk me up as yet another person who read his book back in the day and thought they looked very weird.
Bonus: a Dromeosaur of some kind using her Large Talon to kick the crap out of… a rat, I think. (Though I also like that nearly all his smaller theropods sported feathers.)

I have Mcloughlin’s book, and even though it’s ahead of it’s time in some ways (illustrating small dinosaura as being feathered, long before the real ones came to light) I never liked his depictions of horned dinosaurs with frills encased in skin (or his stegosaurs rolling up in a ball like hedgehogs, for that matter.) I’m glad your anatomical analysis doesn’t support his depiction of ceratopsians, because function aside, it just looks terrible!

Agreed with Ray. And Zach, on the subject of Pachyrhinosaurus and its kin (awesome that the group actually exists though) being one of the more basal centrosaurine groups, you’ll have to ask Dr. Ryan about that.

I’ve read somewhere that centrosaurines may have been more gregarious and preferred drier uplands, while chasmosaurines lived in smaller herds in the moister lowlands (hmm… or was it the other way around).

It was.

I agree, not only does the new style look rather ugly, especially the new font style, but it reminds me too much of Pharyngula,

What? How? Pharyngula has a totally different layout… compared to that, the previous Sb default layout and the new one are almost identical… ~:-|

and its swampload of weird comments, especially about bacon.

How many threads have you read since that open one several weeks ago…?

Next I suppose they’re going to make it mandatory to register to comment on ScienceBlogs.

That has, fortunately, already been abandoned again at Pharyngula. (No idea why. PZ simply said so in the “Easter is for everyone” thread.)

salamanders only have one neck vertebra

That, actually, is normal. Having a longer neck is unique to amniotes or something. 🙂

Pachyrhinosaurinii

Pachyrhinosaurini. 🙂

“Basal” means “far away from the group I’m interested in at the moment. If you’re interested in lizards, it makes sense to say that the mammals are the basalmost extant amniotes, and indeed several papers have said it that way. (Off the top of my head, I think Zardoya & Meyer 1993, on the phylogenetic position of the turtles, do.)

Our museum director (who does NOT keep up with the literature) claims unsubstantiated reports of Late Cretaceous temperatures dipping to 30 below in the winter. I seriously doubt that. Every other piece of data I’ve read suggests that the North Slope of LK Alaska was similar to modern Washington state. This is based mostly on the floral assemblage. Got chilly in the winters with some ice formation, but nothing too severe. Probably no snow. It must have gotten cold enough to keep ecotherms out (no crocs or squamates so far), though.

Darren: Should we assume that by “spherical” you meant “hemispherical”?

I wonder if the frill and hyper-mobile neck joint worked together. Rather than just being a prickly mouthful, maybe the frill’s motion could make it hard for T. rex to focus on where to bite.

I’m guessing there were many defensive strategies that we don’t see much today in the ceratopsians’ modern analogs because they don’t work any more. The large predators of today have much bigger brains, with perceptual apparatus organized such as to be able to counter primitive strategies. Maybe strategies that we see still working against small lizards or cephalopods were effective, then, against large predators. The neuroanatomy and organization of one’s principal predators’ brains must be as important a part of the evolutionary environment as those of one’s mating competitors.

Nathan Myers said
>>>Darren: Should we assume that by “spherical” you meant “hemispherical”?

–My recollection is that it’s a good deal more than hemi: something like ?? 2/3 ?? of a sphere, with only the top third sunk into the mass of bone it’s mounted on. The AMNH in New York has one ceratopsian skull mounted with its top (maybe missing?) to the wall so you get to look at it from a ventral point of view: the occ. cond. is a truly amazing, somewhat bigger than a baseball, object!

Does Witmer’s recent work not suggest that ceratopsians had a very low intelligence? IIRC he states that it is hard to imagine any kind of complex behavior for ceratopsians given their low intelligence. I doubt if a similar conclusion has been reached for the predators of the ceratopsians, the coelurosaurs.

@Zach Miller: Unfortunately Washington state has no animals even close to elephant size, to compare thermoregulation with. I think it would be stretching it in the summer, though, to have fur/feather like coatings. From a quick Googling, it seems that rhinoceroses used to live as far north as mid-northern Pakistan, which can have chilly winters. So probably there’d be no need to develop a coat – it would need to be an innovation; it’d certainly have overheated more southerly ceratopsians.

I wonder if the frill and hyper-mobile neck joint worked together. Rather than just being a prickly mouthful, maybe the frill’s motion could make it hard for T. rex to focus on where to bite.

Why do people keep assuming it would want to bite into the neck? The only mammals that come anywhere close to being comparable to a tyrannosaur are Xenosmilus and maybe the killer whales. I see no reason why it should have wasted time trying to make precision bites with that kind of dentition (and teeth that didn’t occlude in the first place). Isn’t it more likely that it took out the leg muscles with one bite – there’s a great illustration in PDW of how that would work – and then just kept eating?

The large predators of today have much bigger brains

Always be careful with that. Relative brain size depends on absolute body size in interesting ways, and we still don’t know what a bloated brain like ours* is really good for.

* Which, incidentally, is merely at the upper end of the range expected for mammals of our size.

That McLoughlin dinosaur book was always a curiosity to me. Such weird ideas and drawings for a kid who was used to seeing Bill Stout and Zallinger. Oddly enough, the McLoughlin they had at the library was “Synapsida” which I checked out regularly. As much as I disliked “Archosauria”, I adored “Synapsida”. Maybe that affection has to do more with the cover image of all those dinocephalians posing and ripping each other’s throats open.

If I remember correctly, the only other book to advance this model of ceratopsian frills was the terrible (and pace Monty Python, this time I *don’t* mean “terribly violent” Dinosaurs of the Southwest by Ronald Ratkevich.

– “regeneration in dinosaur limbs and tails, skin and muscles covering ceratopsian frills so that they did not stick out from the rest of the body, etc.” — (Also, if I remember correctly, the highest speed estimate I’ve ever seen for T. rex, but I don’t recall the exact number. I want to say either 50mph or 70mph [80kph / 110kph].)

“Ratketvitch’s book is the one that Greg Paul referred to in _Predatory Dinosaurs…_ as ‘possibly the worst dinosaur book ever written’, and frankly I’m rather inclined to agree.”

From a quick Googling, it seems that rhinoceroses used to live as far north as mid-northern Pakistan, which can have chilly winters. So probably there’d be no need to develop a coat – it would need to be an innovation; it’d certainly have overheated more southerly ceratopsians.

Still, we need a good Arctic-ceratopsian skin impression…

(But what was mid-northern Pakistan’s winter like back then.. or did you mean ‘can have had’ chilly winters?)

I am thinking of Hannibal and his elephants crossing the Alps.. issues of cold I think are not solely maintaining core body temp for survival, but of not having too steep a temperature gradient.. maintaining extremities warm enough not to get frostbite trauma.
Wind-chill and radiative heat loss and all that, with bare skin..

Might it get to the point that, to keep surface tissues from freezing trauma, the required continual heat exchange from deeper tissues would demand more energy than available from reserves+food intake available.

Of course penguins and polar bears manage in extremes, but how cold could a ceratopsian tolerate long-term?
Are layers of subcutaneous fat feasibly present and adequate as alternatives, in reptiles, to fur/feathers for coping with extreme cold?
Are there any reptiles known to endure or have endured prolonged extreme cold while remaining active? or did ceratopsians hunker down into a chilled torpor?

I’ve heard some amphibians can be frozen in solid ice yet revive.
B-movie and Disney scenarios notwithstanding, I don’t envisage that for ceratopsians.. but, who knows?!

I have been a professional dinosaur sculptor for over 25 years. Many years ago I was intrigued by the”sub-ducted frill”concept, and,after much discussion with several colleagues,decided to see if it would work in # dimensions. To put it succinctly, it doesn’t. What is not apparent in profile drawings is the width of the frill, which is quite a bit wider than the shoulders! Attempting to bury the frill produces an animal that has almost as much mass ahead of it’s forelegs as behind them, with no ability to move it’s head at all(or lift it off the ground, for that matter!). This is one of the great advantages of sculpting;that third dimension, which brings the silly ideas(like this one) into proper perspective…PS

John McLoughlin’s book was really interesting in his depiction of dinosaurs.(still got my copy somewhere)
The mass of muscle joining the head to the body to resemble a buffalo hump was strange enough, but if you start looking at the rest of the facial structures, his dinosaurs have a real mammalian fleshiness to them.
Coupled with goat like pupils they come across as big bovine sort of creatures.
While this certainly wasn’t and isn’t the prevailing vision for dinosaurs, it certainly embraced the idea of warm blooded animals far removed from reptilian ancestors.

I have been recontructing and illustratiing dinosaurs for 20 years now, and i agree with paul, however it would be interesting if they were THAT weird.
However a little off the subject ..One thing that bothers me that i find to be a common trend among anyone making any speculations one way or another. is this black and white view of functional morphology and its applications. Taking a firm stance one way or another seems to have more to do with ego and drama than it does with science. Nothing in nature is black and white predators are scavengers and vice versa with very few exceptions. Its a mistake to ever assume otherwise It has been stated that ceratopsian frills were not adequate protection against tyranosaurs, while this is fundementally correct it does not take realism into account. yes a T.Rex could bite through bone and get past a Triceratops frill
But simply having an obstacle in the way of a vulnerable area might be enough (in my opinion it is, but Theres always doubt) The oppurtunities for survival that a Tyrannosaur biting into a frill presents are great indeed, In my view this concept is the only thing we can be certain about.
For instance One would argue that the human arm isnt a Viable sheild for anything and Structurally it isnt… but if I am being attacked by a dog for instance You better beleive the fact that i give him my arm to bite instead of my neck is going to give me a VERY valuable oppurtunity to save my life and escape the attack. My arm did not evolve for this purpose it has a countless number of uses and functions that are all Dictated by situation. To choose any one of them as a Single reason for its development in human evolution is Ridiculously ignorant for a scientist to do.
I think that the real problem here is that our understanding of evolution and the forces behind it is incomplete, how then can we make any real educated assumptions? we can but those assumtions stand on severely shaky ground, funny thing is people studying paleontology seem to fancy being ignorant to this, and real science goes out the window, giving way to dramatic characters who are as puzzling outlandish, and Strange as the animals they study.While i find your theories very intriguing I dont think anyone can have the knowlege to agree or disagree
(I get a tiny little grin in amusment of the ignorance and arrogance it takes for some paleontologist to state they agree or disagree with anything absolutely) . My point is simply, this… Be carefull of absolutes in your theories and speculations dont close your mind. The Field of paleontology is in desperate need of more scientist and less ignorant, egotistical, Vanity/attention addicted, clowns having pissing contests, Though it is fun to watch them be proven wrong.